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Abstract

Background

The Dermaptera belongs to a group of winged insects of uncertain relationship within
Polyneoptera, which has expanded anal region and adds numerous anal veins in the hind
wing. Evolutional history and origin of Dermaptera have been in contention.

Results

In this paper, we report two new fossil earwigs in a new family of Bellodermatidae
fam. nov. The fossils were collected from the Jiulongshan Formation (Middle Jurassic)
in Inner Mongolia, northeast China. This new family, characterized by an unexpected
combination of primitive and derived characters, is bridging the missing link between
suborders of Archidermaptera and Eodermaptera. Phylogenetic analyses support the new
family to be a new clade at the base of previously defined Eodermaptera and to be
a stem group of (Eodermaptera+Neodermaptera).

Conclusion

Evolutional history and origin of Dermaptera have been in contention, with dramatically
different viewpoints by contemporary authors. It is suggested that the oldest Dermaptera
might possibly be traced back to the Late Triassic-Early Jurassic and they had divided
into Archidermaptera and (Eodermaptera+Neodermaptera) in the Middle Jurassic.

Background

The earwigs (Dermaptera) are familiar insects, often unwelcomed, mainly due to their
nocturnal habit, some feeding on decaying matters, emitting foul smell, and an unfounded
myth that earwigs would crawl into peoples' ears and penetrate into their brains during
sleep. The Dermaptera belongs to a group of winged insects of uncertain relationship
within Polyneoptera, which has expanded anal region and adds numerous anal veins in
the hind wing [1]. Earwigs are very scarce in the insect fossil record. Nel et al. in 1994 listed only
73 taxa of Dermaptera described, figured or simply mentioned in literature [2]. Even with subsequent addition of 10 species, the fossil record of the Dermaptera
stands at 83 species [3,4]. Evolutional history and origin of Dermaptera have been in contention, especially
for the fossil earwigs.

Here we report a new genus with two new species (Belloderma arcuata gen. et sp. nov. (Figure 1) and Belloderma ovata sp. nov. (Figure 2)) in a new family of Bellodermatidae fam. nov., from the Middle Jurassic (Bathonian-Callovian)
of the Jiulongshan Formation [5-7] in Daohugou (N41°18'30", E119°13'00") of Ningcheng County, Inner Mongolia, China.
Our study of these two earwigs and phylogenetic results provide new understanding
of earwigs' origin and evolutional process and enable us to update the phylogenetic
and evolutional relationships among major lineages of earwigs.

Methods

The specimens were examined with a Leica MZ12.5 dissecting microscope and illustrated
with the aid of a drawing tube attached to the microscope. Line drawings were made
with photoshop9.0 graphics software. Morphological terms used here follow those by
Michael S. Engel and Fabian Haas [8].

Phylogenetic Analysis

The relationships of fossil Dermaptera is re-assessed, the fossil taxa used in the
phylogenetic analyses of fossil Dermaptera are listed in Table 1. This study predominantly used body characters, because wing characters and male
genitalia characters are almost always poorly preserved in fossils. We followed the
original descriptions because these fossils were not available to us. Our phylogenetic
analyses of Dermaptera used limited characters to study the reliability and position
of the new family Bellodermatidae fam. nov. rather than the inter-relationships of
Dermaptera. Thus, if a fossil earwig genus contains several species, only one representative
species was chosen to keep the number of taxa low for computational reasons. The character
matrix for this dataset is shown in Table 2 and Table 3. We constructed matrices with 17 taxa, 20 characters and 20 taxa, 20 characters separately.
The two matrices are the same for the fossil species, but they are different in three
additional extant taxa in Table 3. Three species of Blattodea (Leucophaea maderae, Polyphaga aegyptiaca, Periplaneta americana) and a species of Plecoptera (Isoperla obscura) [9-11] are used as outgroup.

All characters were treated as unordered and weighted equally. The data matrices were
subjected to the parsimony analyses in NONA and PAUP* (version 4.0b10) [12]. The two programs implement heuristic searches somewhat differently, and so both
were employed. Because program NONA can be only defined one outgroup, so we conducted
the cladistic analyses by each outgroups respectively. Heuristic search in WinClada/NONA
used multiple random additions of taxa and tree-bisection resection branch swapping
(options set to hold 10000 trees, perform 1000 replications with one starting tree
replication, and the multiple TBR+TBR search strategy). Heuristic search in PAUP*
(version 4.0b10) employed a heuristic parsimony analyses, with 1000 random stepwise
additions of taxa (TBR branch swapping) under ACCTRAN optimization.

To comply with regulations of the International Code of Zoological Nomenclature (ICZN),
we have deposited paper copies of the above article at the Natural History Museum,
London; the American Museum of Natural History, New York; the Muséum National d'Histoire
Naturelle, Paris; the Russian Academy of Sciences, Moscow; and the Academia Sinica,
Taipei.

List of characters and character states for phylogenetic analysis (*: only present
in matrix of Table 3)

1. Head. Opisthognathous (0) or prognathous (1) [13]. The three blattodean species have opisthognathous head, while all other taxa possess
a prognathous head.

2. Antennomere. 1st longer than 2nd (0) or 1st shorter than or equal to 2nd (1) (Own
observation). Character state 1 is present in Archidermapteron, Asiodiplatys, Protodiplatys, Microdiplatys, Longicerciata; all other species have character state 0.

3. Hind margin of head. Relatively straight (0) or strongly notched (1) (Own observation).
The hind margin of head is strongly notched in Isoperla, Archidermapteron, Belloderma gen. nov, Semenoviola, Semenovioloides, *Forficula and *Anechura; the hind margin of head in all other taxa is relatively straight. This character
state is uncertain in blattodean species.

4. Neck. Blattoid-type (0) or forficuloid-type (1) [13,14]. The three blattodean species possess a blattoid-type neck; all other examined dermapterans
possess a forficuloid-type neck.

5. Shape of pronotum. Disc-like, large, Blattodea-type (0) or disc-like, small, Dermaptera-type
(1) [13]. All dermapteran species have disc-like, small, Dermaptera-type pronotum, while being
large in three blattodean species.

6. Venation of tegmina. Present (0) or absent (1) (Own observation). Veins are absent
in *Archaeosoma, *Forficula and *Anechura; while all other species have veins in their tegmina.

7. Shape of tegmina. Long, outer margin produced into a point (0) or short, apically
blunt (1) (Own observation). The tegmina are long and outer margin produced into a
point in three blattodean species, Isoperla, Belloderma gen. nov, Dermapteron, Jurassimedeola, Sinopalaeodermata, Semenoviola and Semenovioloides; all other have short and apically blunt tegmina.

8. Spiny crest on tegmina. Absent (0) or present (1) [13,14]. The spiny crest is absent in three blattodean species and Isoperla, but present in the dermapterans.

9. Hindwing. Long, folded, fan-like (0) or with two transverse folds (1) [13]. A wing package with two transverse folds is present in all fossil and extant Dermaptera,
while three Blattodea species and Isoperla have a simple, fan-like, folded wing.

10. Broadening. Absent (0) or present (1) [13]. The broadenings are present in all fossil and extant Dermaptera, but is absent in
the three blattodean species and Isoperla.

11. Spines on femoral carina. Absent (0) or present (1) [13]. Spines are present in Archidermapteron, Asiodiplatys, Longicerciata, Microdiplatys, Protodiplatys; they are absent in all other species.

12. Number of tarsomeres. Five (0) or three (1) [13]. There are tarsi with five tarsomeres in three blattodean species, Archidermapteron, Asiodiplatys, Dermapteron, Jurassimedeola, Longicerciata, Microdiplatys,
Protodiplatys, Sinopalaeodermata and Turanovia; all other species have 3 tarsomeres.

15. 8th and 9th abdominal tergites in females. Distinct and separate from 10th tergite
(0), narrowed, but separate from 10th tergite and not covered by 7th tergite (1) or
fused to 10th tergite and covered by 7th (2) [13]. The tergites are distinct and separate in three blattodean species, Isoperla, Archidermapteron, Asiodiplatys, Dermapteron, Jurassimedeola, Longicerciata, Microdiplatys, Protodiplatys,
Sinopalaeodermata and Turanovia; the tergites are narrowed in *Archaeosoma, Belloderma gen. nov, Semenoviola, Semenovioloides, Turanoderma; the state 2 is present in *Forficula and *Anechura.

16. Length of cerci. shorter than (0) or longer than abdomen (1) [13]. Character state 1 is present in Archidermapteron, Asiodiplatys, Protodiplatys, Microdiplatys and Longicerciata; character state 0 is present in other species.

18. Shape of adult cerci. Straight (0) or evenly curved (1) (Own observation). The
cerci are evenly curved in Turanoderma, Turanovia, *Archaeosoma, *Forficula and *Anechura; the cerci of other species are straight except Semenoviola, which is uncertain for this character because of poor preservation.

19. Structure of adult cerci. Symmetrical (0) or asymmetrical (1) (Own observation).
The adult cerci are symmetrical in all examined species except Belloderma gen. nov, which have asymmetrical cerci.

20. Ovipositor. Exposed (0) or unexposed (1) [13]. The ovipositor is unexposed in outgroup, *Forficula and *Anechura; all other species have an exposed ovipositor, except *Archaeosoma, Dermapteron, Longicerciata, Semenoviola and Semenovioloides because the known fossils are male or poor preserved.

Holotype: CNU-Der-NN2008002 (coll. Shih Chungkun), an almost complete specimen, is housed
in the Key Lab of Insect Evolution & Environmental Changes, the College of Life Sciences,
Capital Normal University (CNU), Beijing.

Legs: Length ratio of foreleg femur: tibia: tarsus is 1.2:1.2:0.9, and 1.3:1.6:1.1
for midleg. Mid-femur nearly as long as or slightly longer than fore-femur, hind-femur
longest. Tibiae slender and longer than femora, with bristle on external surface.
Tarsi 3-segmented and although not as stout as tibiae, 1st segment long and stout,
2nd shortest, and 3rd longest; pre-tarsal claws well-developed and long, arolium absent.
Hind-coxa long, no tibia and tarsus preserved.

Wing: Tegmina about 3 times as long as wide, extending backwards to 2nd abdominal
segment; widest aspect lying near basal third, with its outer margin and costal margin
strongly arched, a distinct character of the most basal fossil dermapterans, inner
margin straight and overlapping. A small distal section of Rs and M visible, other
longitudinal veins unclear.

Thorax: Pronotum about 1.8 times as wide as long. Meso-sternum rectangular, with rounded
corners. Meta-sternum large and semicircular. Tegmina poorly preserved and only a
small section of M and Cu visible, Cu with two branches (CuA and CuP) with CuP straight
and CuA arched.

Legs: Length ratio of foreleg femur: tibia: tarsus is 1.2:1.3:0.5, and 1.4:1.4:0.9
for midleg. Legs almost the same as Belloderma arcuata gen. et sp. nov.

Remarks

The two species are very similar to each other in body size and eye size, but they
differ from each other by shape of the pronotum, pro-sternum and abdominal segments,
and they have distinctly different tegmina shapes.

A new family is erected based on these two well-preserved, unique fossil specimens
with an unexpected combination of characters (Table 4). The combined characters of this new family allow its allocation to the suborder
Eodermaptera: tarsi three-segmented, tegmina retain venation, 8th and 9th abdominal
tergite in females are narrowed, but separate from 10th tergite and not covered by
7th tergite and exposed ovipositor. However, there are some particular features of
the new family, which are not present for other fossils of Eodermaptera. For instance,
the cerci are segmented, which makes the new family be strikingly analogous to the
species of suborder Archidermaptera. On the other hand, the new family has a character
assemblage similar to extant insects in Neodermaptera, namely, tarsi three-segmented,
and 1st segment long and stout, 2nd shortest and distinctly extended distally beneath
3rd one (forficulid-type). The tarsi character is an important family character in
the classification of Dermaptera. The species of Dermapteridae of suborder Archidermaptera
has 5 tarsi segments for fore, middle and hind legs, i.e. 5-5-5. The tarsi segments
of Protodiplatidae of suborder Archidermaptera are 4-4-5, Semenoviolidae and Turanodermatidae
of suborder Eodermaptera and all extant earwigs possess tarsi with three tarsomeres,
3-3-3, of which the shape of the 2nd segment is considered as a family character.
With respect to tarsi, the new family is close to the modern Dermaptera [1].

In summary, the above-mentioned characters show that the placement of the new family
to the suborder Eodermaptera is dubious. To make sure its exact placement, we set
up two matrices and carried out phylogenetic analyses, one with only fossil taxa and
the other with fossil and three representatives of extant taxa.

Results of phylogenetic analyses

The phylogenetic analyses of Table 2 by NONA, we get four most parsimonious trees, tree length = 25, consistency index
= 0.76, retention index = 0.89 (Figure 3a), and by PAUP, we get 34 most parsimonious trees, tree length = 25, consistency index
= 0.7600, retention index = 0.8966 (See Additional file 1). The phylogenetic analyses of Table 3 by NONA, we get two most parsimonious trees, tree length = 31, consistency index
= 0.67, retention index = 0.87 (Figure 3b), and by PAUP, we get four most parsimonious trees, tree length = 31, consistency
index = 0.6774, retention index = 0.8780 (See Additional file 2). The results by the two programs are similar, and results conducted by NONA with
the species of Blattodea as outgroup are same (See Additional file 3). The best supported trees are shown in Figure 3.

Figure 3.Phylogenetic analysis (results of NONA with Isoperla as outgroup). a, Strict consensus tree from Table 2 by NONA (Topology of strict consensus tree
by PAUP is same to NONA, see Additional file 1, Fig S1); b, Strict consensus tree from Table 3 by NONA (Topology of strict consensus
tree by PAUP is slightly different to NONA, see Additional file 2, Fig S2); c, One most parsimonious tree from Table 3 by NONA. Other results by NONA
are same (see Additional file 3, Fig S3).

Additional file 1.Fig S1: Strict consensus tree from Table 1 by PAUP. Result of cladistic analysis by PAUP based on Table 2.

Phylogenetic analyses show that the order Dermaptera is divided into two clades: Archidermaptera
and Eodermaptera (or Eodermaptera+Neodermaptera, in the analyses including of the
extant groups) (Figures 3a, b). The monophyly of Archidermaptera is confirmed in all the analyses, supported by
two synapomorphies: straight hind margin of head (Cha. 3: 0) and pleural overlapping
of abdominal tergites and sternites (Cha. 14: 1) (Figures 3a, b, c). The suborder Eodermaptera is well assembled in the analyses that is only concerned
for the fossil taxa, supported by one synapomorphic character: fusion of 8th and 9th
abdominal tergites in females (Cha. 15: 1) (Figure 3a). However in the analysis including the extant representatives, Eodermaptera grouping
with Neodermaptera constitute a monophyly, sharing with Cha. 15 (Figure 3c). Although it resulted in some different cladograms, our new family is firmly assigned
to the Eodermaptera or (Eodermaptera+Neodermaptera), representing a stem-group of
the clade.

Discussion

About the suborder Eodermaptera

Earwigs from the Jurassic were usually classified in the extinct suborder Archidermaptera,
comprising the known basalmost lineage, which persisted until the earliest Cretaceous
[15-18]. The genus Semenoviola Martynov, 1925 was placed in Coleoptera when it was erected, then it was transferred
to Pygidicranidae Verhoeff, 1902 together with Semenoviolidae and Turanodermidae,
which is a family of known Neodermaptera [16]. Besides, as demonstrated by Willmann [17] and Haas and Kukalova-Peck [13], the Semenoviolidae and Turanodermidae are more closely allied to suborder Neodermaptera
owing to the unsegmented cerci but excluded from the latter owing to the plesicmorphic
retention of venation in the tegmina. For this reason, Engel [19] proposed a new name, Eodermaptera, including Semenoviolidae and Turanodermidae. According
to the phylogenetic analyses here, the so-called suborder Eodermaptera becomes paraphyletic,
and so we considered that the previously defined Eodermaptera species should be returned
to the Neodermaptera or to combine them together as a new classification group.

About the evolutional history and origin of Dermaptera

Evolutional history and origin of Dermaptera have been in contention, with dramatically
different viewpoints by contemporary authors. Some experts suggested the oldest fossils
to date are tegmina from the Late Triassic of England and Australia [20], but because of the poor preservation, others suggested the Dermaptera probably originated
during early Mesozoic in Asia [21].

Our study of these earwigs and phylogenetic results have shed light on evolutional
process and origin. The Dermapteridae species have 5-5-5 tarsi, the same as Protelytroptera,
Protodiplatyidae species have 4-4-5 tarsi, and then (Eodermaptera+Neodermaptera) species
have 3-3-3 taici. On the other hand, the unique nature of hind wing in Dermapteridae
indicates a closer relationship with Protelytridae among Protelytroptera, which is
considered as the ancestor of Dermaptera. The afore-mentioned summary shows that Dermapteridae
is the most basal in the Dermaptera and they are present in Middle Jurassic. Protodiplatyidae
was discovered only from the Late Jurassic [16,18]. The more derived Bellodermatidae fam. nov. was present in the Middle Jurassic of
Jiulongshan Formation in Daohugou. Therefore, it is suggested that the oldest Dermaptera
might possibly be traced back to the Late Triassic-Early Jurassic and they had divided
into Archidermaptera and (Eodermaptera+Neodermaptera) not later than Early Jurassic.

The Turanodermatidae is presently known only from the Late Jurassic of Central Asia
but may extend to the Early Cretaceous if the genus Archaeosoma [18] proves to be allied [19]. In Figure 3c, phylogenetic analysis shows that character 3 weakly supports the combination of
Archaeosoma and Turanoderma to be Turanodermatidae, but in the strict consensus tree, namely Figure 3b, Archaeosoma and Turanoderma are paraphyletic, so further research is needed about whether the genus Archaeosoma can be allied to the family Turanodermatidae. The previously known eodermapterans
up to date have been documented only from the Late Jurassic of Karatau in Chimkent
Province of Kazakhstan [13]. The discovery of Bellodermatidae fam. nov. extends the age of previous Eodermapptera
to the Middle Jurassic.

The previous neodermapterans first appear in the Early Cretaceous [22,23] but might have originated in the Late Jurassic [24]. Certainly, definitive neodermapterans and recognizable pygidicranids are known by
the Middle Cretaceous [1,25]. In summary, following Grimaldi and Engel [1], the evolution of Dermaptera is updated in Figure 4.

Conclusions

This new family Bellodermatidae fam. nov., bridging the missing link between suborders
of Archidermaptera and Eodermaptera greatly enhanced the understandings of early evolution
of Dermaptera. Based on the phylogenetic analysis, the new family is attributed to
the Eodermaptera or (Eodermaptera+Neodermaptera) unambiguously, representing a stem-group
of the clade. The suborder Eodermaptera becomes paraphyletic with Neodermaptera, and
the previously defined Eodermaptera species should be returned to Neodermaptera or
to combine them together. It is suggested that the oldest Dermaptera might possibly
be traced back to the Late Triassic-Early Jurassic and they had divided into Archidermaptera
and (Eodermaptera+Neodermaptera) in the Middle Jurassic.

Authors' contributions

JZ carried out the fossil processing, photography, figure preparation, data analysis
and interpretation, manuscript drafting and finalization. YZ, CS & DR did the fieldwork,
collected the specimens, participated in the data analysis and interpretation, and
manuscript modification. YW participated in the data analysis and interpretation,
and manuscript modification. All authors read and approved the final manuscript.

Acknowledgements

We thank Dr. Jinzhong Fu, Dr. Lihong Tu and Dr. Yunzhi Yao for phylogenetic analyses,
Steve Davis for improving the manuscript, Wenying Wu and Qiang Yang for collecting
references. This research was supported by the National Natural Science Foundation
of China (No.40872022, 30811120038, 31071964), the Nature Science Foundation of Beijing
(No.5082002) and Scientific Research Key Program KZ200910028005 and PHR Project of
Beijing Municipal Commission of Education.